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Pathogenesis and Immunity

JC Virus-Specific Immune Responses in Human Immunodeficiency Virus Type 1 Patients with Progressive Multifocal Leukoencephalopathy

Nina Khanna, Marcel Wolbers, Nicolas J. Mueller, Christian Garzoni, Renaud A. Du Pasquier, Christoph A. Fux, Pietro Vernazza, Enos Bernasconi, Raphael Viscidi, Manuel Battegay, Hans H. Hirsch, ; for the Swiss HIV Cohort Study
Nina Khanna
1Division of Infectious Diseases and Hospital Epidemiology, University Hospital Basel, CH-4031 Basel, Switzerland
2Institute for Medical Microbiology, Department of Biomedicine, University of Basel, CH-4003 Basel, Switzerland
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Marcel Wolbers
3Institute for Clinical Epidemiology and Biostatistics, University Hospital Basel, CH-4031 Basel, Switzerland
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Nicolas J. Mueller
4Division of Infectious Diseases and Hospital Epidemiology, University Hospital Zurich, CH-8091 Zurich, Switzerland
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Christian Garzoni
5Division of Infectious Diseases and Laboratory of Virology, University Hospital Geneva, CH-1205 Geneva, Switzerland
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Renaud A. Du Pasquier
6Divisions of Neurology and Immunology, Centre Hospitalier Universitaire Vaudois, CH-1011 Lausanne, Switzerland
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Christoph A. Fux
7Division of Infectious Diseases, University Hospital and University of Bern, CH-3010 Bern, Switzerland
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Pietro Vernazza
8Department of Internal Medicine, Cantonal Hospital, CH-9000 St. Gallen, Switzerland
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Enos Bernasconi
9Department of Internal Medicine, Regional Hospital, CH-6900 Lugano, Switzerland
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Raphael Viscidi
10Stanley Division of Developmental Neurovirology, Department of Pediatrics, Johns Hopkins University School of Medicine, Baltimore, Maryland
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Manuel Battegay
1Division of Infectious Diseases and Hospital Epidemiology, University Hospital Basel, CH-4031 Basel, Switzerland
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Hans H. Hirsch
1Division of Infectious Diseases and Hospital Epidemiology, University Hospital Basel, CH-4031 Basel, Switzerland
2Institute for Medical Microbiology, Department of Biomedicine, University of Basel, CH-4003 Basel, Switzerland
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  • For correspondence: Hans.Hirsch@unibas.ch
DOI: 10.1128/JVI.02657-08
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  • FIG. 1.
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    FIG. 1.

    Laboratory markers over time in PML survivors and nonsurvivors: HIV viral load (copies/ml), CD4+ T-cell count (cells/μl), JCV- and CMV-specific cellular immune responses (gamma interferon SFU/million PBMCs), and JCV-specific IgG and IgM antibody activities (OD492).

  • FIG. 2.
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    FIG. 2.

    Cellular and humoral immunities in PML cases at the time of PML diagnosis and in matched controls. The P values correspond to comparisons of cases versus controls in PML survivors and nonsurvivors separately with adjustment for matching as described in Materials and Methods. The box plots of data are drawn in gray, with individual measurements shown as black dots.

Tables

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  • TABLE 1.

    Baseline characteristics for 29 PML cases

    CharacteristicsaSummary statisticbPc
    All patients (n = 29)Survivors (n = 18)Nonsurvivors (n = 11)
    Age (yr)39 (36, 45)37 (34, 44)42 (39, 45)0.13
    Female gender5 (17)2 (11)3 (27)0.34
    PML diagnosis
        Definitive4 (14)2 (11)2 (18)0.09
        Laboratory confirmed10 (34)4 (22)6 (55)
        Possible15 (52)12 (67)3 (27)
    Yr since first positive HIV test8.20 (2.72, 11.34)7.10 (0.51, 9.14)10.81 (8.30,13.19)0.03
    CD4 cell count (cells/μl)102 (35, 152)119 (82, 192)35 (18, 107)0.02
    CD8 cell count (cells/μl)700 (455, 1137)698 (546, 1030)700 (425, 1168)0.74
    HIV viral load (log10 copies/ml)4.18 (2.62, 5.28)3.88 (2.62, 4.88)4.98 (2.79, 5.41)0.22
    Prior AIDS-defining conditions12 (41)9 (50)3 (27)0.27
    cART status at PML diagnosis
        cART naïve10 (34)7 (39)3 (27)0.45
        cART treated10 (34)7 (39)3 (27)
        cART interrupted9 (31)4 (22)5 (45)
    cART (re)initiated within 3 mo of PML diagnosis
        In cART-naïve patients7/10 (70)6/7 (86)1/3 (33)0.10
        In cART-pretreated patients4/9 (44)3/4 (75)1/5 (20)
    • ↵ a Time-dependent covariates evaluated at the time of PML diagnosis.

    • ↵ b Median (IQR) for continuous variables; n (%) for categorical variables.

    • ↵ c Survivors versus nonsurvivors; based on Wilcoxon test for continuous variables and Fisher's exact test for categorical variables.

  • TABLE 2.

    Comparison of PML cases and their matched controlsa

    ParameterAll PML patients and their controlsPatients with laboratory-confirmed or definitive diagnosis and their controls
    Odds ratio (95% CI)POdds ratio (95% CI)P
    JCV-specific cellular immune response (estimates by 10-fold higher of parameter +1)
        All patients0.77 (0.36, 1.62)0.480.20 (0.03, 0.68)0.008
        Survivors1.19 (0.48, 3.05)0.710.50 (0.09, 2.08)0.34
        Nonsurvivors0.29 (0.05, 1.13)0.080.03 (0.00, 0.46)0.004
    CMV-specific cellular immune response (estimates by 10-fold higher of parameter +1)
        All patients0.85 (0.46, 1.54)0.600.56 (0.19, 1.47)0.24
        Survivors0.87 (0.35, 2.07)0.751.41 (0.18, 11.50)0.73
        Nonsurvivors0.85 (0.38, 1.88)0.680.44 (0.11, 1.30)0.14
    JCV VLP IgG response (estimates by 2-fold-higher parameter value)
        All patients1.31 (1.01,1.75)0.041.14 (0.83, 1.63)0.42
        Survivorsb1.73 (1.19, 2.70)0.0031.46 (0.91, 2.94)0.13
        Nonsurvivors0.86 (0.53, 1.34)0.500.88 (0.52, 1.43)0.62
    JCV VLP IgM response (estimates by 2-fold-higher parameter value)
        All patients1.45 (0.91, 2.40)0.122.39 (0.99, 6.24)0.053
        Survivors1.44 (0.87,2.48)0.153.08 (1.02, 11.11)0.047
        Nonsurvivors1.48 (0.41, 5.32)0.531.51 (0.35, 6.65)0.56
    • ↵ a Odds of developing PML based on cellular and humoral immunity at time zero in all patients and in PML survivors and nonsurvivors (and their matched controls) separately. The results are based on logistic regression using Firth's bias reduction adjusted for matching. CI, confidence interval.

    • ↵ b If results are based on non-log-transformed JCV VLP IgG response instead, which is equally sensible based on the data, the results for survivors are significant both in all survivors (P = 0.001) and in survivors with laboratory-confirmed or definitive diagnosis and their controls (P = 0.03).

  • TABLE 3.

    Logistic survival for estimating the effects of cellular and humoral immunity at the time of PML diagnosis on 1-year survivala

    ParameterAll PML patientsPatients with laboratory-confirmed or definitive diagnosis
    Odds ratio (95% CI)POdds ratio (95% CI)P
    JCV-specific cellular immune response (estimates by 10-fold higher of parameter +1)
        Unadjusted0.36 (0.09, 1.20)0.100.06 (0.00, 0.62)0.02
        Adjusted for CD4 cell count0.45 (0.11, 1.57)0.210.11 (0.00, 1.56)0.11
    CMV-specific cellular immune response (estimates by 10-fold higher of parameter +1)
        Unadjusted1.00 (0.46, 2.19)1.000.67 (0.12, 2.00)0.49
        Adjusted for CD4 cell count1.23 (0.53, 3.04)0.631.15 (0.13, 19.97)0.88
    JCV VLP IgG response (estimates by 2-fold-higher parameter value)
        Unadjusted0.51 (0.27, 0.84)0.0070.62 (0.30, 1.08)0.09
        Adjusted for CD4 cell count0.54 (0.28, 0.90)0.020.67 (0.28, 1.31)0.24
    JCV VLP IgM response (estimates by 2-fold-higher parameter value)
        Unadjusted0.84 (0.34, 1.49)0.580.46 (0.12, 1.39)0.17
        Adjusted for CD4 cell count0.88 (0.36, 1.57)0.680.29 (0.00, 1.30)0.12
    • ↵ a Univariate analyses and analyses adjusted for CD4 cell counts based on logistic regression using Firth's bias reduction. CI, confidence interval.

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JC Virus-Specific Immune Responses in Human Immunodeficiency Virus Type 1 Patients with Progressive Multifocal Leukoencephalopathy
Nina Khanna, Marcel Wolbers, Nicolas J. Mueller, Christian Garzoni, Renaud A. Du Pasquier, Christoph A. Fux, Pietro Vernazza, Enos Bernasconi, Raphael Viscidi, Manuel Battegay, Hans H. Hirsch for the Swiss HIV Cohort Study
Journal of Virology Apr 2009, 83 (9) 4404-4411; DOI: 10.1128/JVI.02657-08

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JC Virus-Specific Immune Responses in Human Immunodeficiency Virus Type 1 Patients with Progressive Multifocal Leukoencephalopathy
Nina Khanna, Marcel Wolbers, Nicolas J. Mueller, Christian Garzoni, Renaud A. Du Pasquier, Christoph A. Fux, Pietro Vernazza, Enos Bernasconi, Raphael Viscidi, Manuel Battegay, Hans H. Hirsch for the Swiss HIV Cohort Study
Journal of Virology Apr 2009, 83 (9) 4404-4411; DOI: 10.1128/JVI.02657-08
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    • ABSTRACT
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KEYWORDS

HIV Infections
HIV-1
JC virus
Leukoencephalopathy, Progressive Multifocal

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